The medical evaluation of patients with balance and equilibrium complaints often includes an assessment of their vestibular function. The goal of this assessment is to determine if peripheral vestibular function is normal or abnormal. If vestibular function is found to be abnormal, is one ear involved or are both ears affected? How severe is the abnormality? Is the abnormality stable or fluctuating? Standard clinical tests frequently do not provide adequate answers to one or all of these questions.
Conventional clinical rotation testing typically uses sinusoidal or velocity step motion with moderate stimulus amplitudes (50-100°/s peak velocity) to assess vestibular function by providing a natural rotational stimulus to the semicircular canals and measuring eye movements evoked by the vestibulo-ocular reflex (VOR). Conventional rotation testing has good test-retest reliability, but relatively low sensitivity. Testing sometimes fails to detect a vestibular abnormality or, if an abnormality is detected, to provide a detailed assessment of the severity and/or the side of lesion.
Quantitative assessment of vestibular function relies primarily on measurements of reflexive eye movements (i.e. the VOR) evoked by either natural or artificial stimulation of the vestibular receptors of the inner ear. Visual acuity is maintained during head movement by the generation of compensatory eye movements that maintain the direction of gaze fixed in space. In the light, the VOR, smooth pursuit, and optokinetic reflex systems work together to generate these compensatory eye movements. But in darkness, compensatory eye movements are generated only by the VOR. Therefore, measurements of VOR eye movements in the dark (or sometimes using high frequency head motions where visual reflexes are ineffective) provide an indirect means of assessing peripheral vestibular function.
There are four clinical tests of the vestibular system currently in use on a regular basis. They each have limitations in reliability, applicability, diagnostic precision, and costs that the new rotation test stimulus and analysis method overcome.
There are two main quantitative clinical tests based on VOR measures: caloric and rotation. Rotation testing includes both conventional passive rotations (sometimes referred to as slow harmonic acceleration or SHA testing) and active, subject initiated autorotation tests. More recently, the “head impulse test” or “Halmagyi head thrust” test has become popular as an easily applied qualitative method for detecting the existence of bilateral or unilateral vestibular dysfunction. These various tests, including their advantages and limitations, are described in more detail below.
Caloric test. The caloric test artificially stimulates the inner ear vestibular receptors using either warm-water or cold-water irrigations of the external ear canals. This evokes eye movements, which are measured and compared across ears to determine vestibular asymmetry. Patients are placed in a supine position with the head elevated about 30° in a darkened room. This head position places one set of vestibular receptors, the horizontal semicircular canals, into an earth-vertical orientation. An irrigation creates a thermal gradient across the inner ear that stimulates the horizontal canal, primarily by inducing a convective fluid movement within the distal loop of the canal, and secondarily, by direct thermal effects. This fluid movement stimulates receptor hair cells, which in turn modulate the activity of the 8th nerve afferents that innervate the horizontal canal. A warm water irrigation results in an increased afferent discharge rate, and a cold water irrigation causes a decreased discharge rate. The increased discharge caused by warm irrigations evokes a sensation of sustained rotation toward the irrigated ear and evokes a compensatory VOR eye rotation away from the irrigated ear. Cold water irrigations evoke oppositely directed sensations and compensatory eye movements.
“Slow phase” compensatory eye movements are interspersed with “fast phase” eye movements that reset the eye position towards the straight ahead gaze position, producing a triangular-shaped eye position waveform referred to as vestibular-evoked “nystagmus.” To quantify this response, the slow phase and fast phase components are separated from one another. The slow phase component is analyzed by calculating its slope which gives the slow phase eye velocity (units °/s) for each beat of nystagmus. The peak velocity is taken as a measure of the responsiveness of the ear to a particular irrigation.
A complete caloric test typically consists of measuring the peak velocity response to four separate irrigations (both warm and cold irrigations in each of the two ears). These four peak velocity measures are scored by the calculation of Jongkees' percentage measures of “reduced vestibular response” (RVR), sometimes referred to as canal paresis, and “directional preponderance” (DP) (See reference 35 listed below). If responses are significantly different in the two ears (typically RVR greater than 25% difference), the ear with the lower response is typically considered to be abnormal. If all four irrigations produce below normal or absent responses, this implies that the patient may have bilaterally reduced or absent vestibular function. The DP measure compares the responses of irrigations that produce right-beating nystagmus with those that produce left-beating nystagmus. If DP is abnormal (typically greater than 25%), this suggests that some non-specific uncompensated imbalance of vestibular function is present.
The chief advantage of the caloric test is that each ear is stimulated individually. This allows for the identification of reduced vestibular function in an ear even though the patient might be well compensated for the lesion and may not express any other overt signs of an acute vestibular lesion. In addition, the RVR and DP measures are quantitative in nature and can be used to grade the severity of the vestibular asymmetry.
Caloric testing has several significant limitations. The thermal stimulus that reaches the inner ear depends upon many anatomical factors (i.e., temporal bone thickness, dimensions of middle ear space, fluid in the middle ear space, variation in blood flow) and procedural factors such as the technician's skill. As a result, there is high variability across subjects in delivery of the thermal stimulus to the inner ear, due to differences in temporal bone thickness dimensions of middle ear space, fluid in the middle ear space, and variations in blood flow. These factors make it difficult to detect small differences in responses between both ears. The end result is that test-retest reliability is poor, making the test a poor choice (unsuitable) for tracking changes in vestibular function over time. In addition, response variability limits the detection of small differences in responses between the two ears. The identification of bilateral vestibular loss is also uncertain due to the wide variations in response amplitudes in a normal population. Finally, the unusual nature of the stimulus (evoking sensations of a long duration rotational motion in a supine position that conflicts with gravity cues from the otolith organs of the inner ear) often provokes nausea in subjects (poor tolerance by subjects) susceptible to motion sickness.
Conventional Rotation Test. The conventional rotation test involves a patient being rotated upright in a clinical rotation chair in a completely dark room. The chair is rotated about an earth-vertical axis, with rotations of moderate amplitude (50-100°/s peak velocity). The typical rotations are sinusoidal, with frequencies ranging from 0.01 to 1.0 Hz. Rotational velocity step stimuli and sometimes pseudorandom or sum-of-sines stimuli are also used.
Rotation testing differs from caloric testing in that a natural rotational stimulus, which stimulates both ears simultaneously, is used to evoke compensatory VOR eye movements. Patients are tested in a completely dark room to eliminate visually generated eye movements. During testing, they are seated upright in a chair mounted on a servo-controlled motor. The motor delivers accurately controlled rotational motions of the chair about an earth-vertical axis. This motion stimulates primarily the horizontal semicircular canals in both ears. In a subject with normal vestibular function, a rotation towards the right causes an increased neural discharge rate in 8th nerve afferents innervating the right side horizontal canal, and a decreased discharge rate in afferents innervating the left horizontal canal. The opposite occurs for rotations to the left. The central nervous system (CNS) uses this “push-pull” neural activity in the two ears to generate VOR eye movements in a direction opposite to the head rotation.
Conventional rotation testing uses rotations with moderate amplitudes (50-100°/s peak velocity). The motion profiles typically are sinusoidal with frequencies ranging from 0.01 to 1.0 Hz [54,59]. Rotational velocity step stimuli [5,32], and sometimes pseudorandom or sum-of-sines stimuli are also utilized [10,47]. Rotation-evoked nystagmus is analyzed in a manner similar to caloric-evoked nystagmus. The nystagmus is separated into slow and fast phase components. The slope of the compensatory slow phase component provides a measure of the slow phase eye velocity over time. With sinusoidal stimulation, this slow phase eye velocity component is sinusoidally modulated at the stimulus frequency. A sinusoidal curve fit to the eye velocity gives quantitative measures of the VOR response that include: VOR gain (response amplitude divided by stimulus amplitude), VOR phase (timing of the response relative to the stimulus), VOR bias (average value of slow phase eye velocity over a complete stimulus cycle), and VOR gain asymmetry (comparison of VOR gain during rotation to the right versus rotation to the left). These response parameters vary as a function of the stimulus frequency, and deviations from the normal pattern are indicative of different types of vestibular dysfunction. For example, normal VOR gain with abnormal phase advance at lower test frequencies, and normal response symmetry is associated with a well compensated unilateral vestibular loss. Reduced VOR gain with abnormal phase advance and normal symmetry indicates a bilateral vestibular loss with the reduction in gain related to the severity of the bilateral loss.
The natural stimulus used by rotation testing, and the precise means available for delivering the rotational stimulus, provide several advantages over caloric testing. First, the test-retest reliability of rotation testing is good, making rotation testing amenable to tracking function over time. Second, the rotation test VOR gain measure has a limited range of normal values, making rotation testing particularly useful in assessing bilateral loss of vestibular function. Third, for sinusoidal rotation tests, the repetitive nature of the stimulus affords great opportunity to use averaging to improve test reliability and the possibility to obtain useful results from partially corrupted data records. Fourth, rotation testing is well tolerated by nearly all patients and only rarely evokes nausea.
The chief disadvantage of rotation testing is that it often does not provide reliable information (inability to provide reliable information) about which ear is abnormal in a patient with unilateral vestibular dysfunction. There are two main reasons for this failure. First, animal studies indicate that the 8th nerve vestibular afferents have a high resting discharge rate averaging about 90 impulses/s. Therefore, for the moderate stimulus amplitudes used in conventional rotation testing, each ear is able to accurately encode bidirectional head rotations without driving the discharge rate of a significant number of neurons to zero during any portion of the sinusoidal stimulus cycle. That is, even if vestibular function is completely absent in one ear, the other ear is able to accurately encode bidirectional head movements, and the CNS is therefore able to generate an accurate VOR. Second, the CNS is able to compensate for the acute effects of a unilateral loss of vestibular function which might otherwise be used to identify the existence of a unilateral vestibular deficit. Specifically, an acute loss of vestibular function results in a strong “spontaneous nystagmus.” This nystagmus occurs because the CNS normally compares the neural activity in the two ears and generates compensatory eye movements proportional to the difference in activity between the two ears. This spontaneous nystagmus typically diminishes over a time course of several days as the CNS rebalances the central VOR neural mechanisms. Once this rebalancing is achieved, only minor signs of vestibular dysfunction remain in the results of conventional rotation tests (specifically, low frequency phase advance, and occasionally, gain asymmetries), and even these minor signs have not been found to reliably indicate the side of the lesion.
A second important limitation in rotation testing is its poor sensitivity in detecting a compensated partial unilateral vestibular loss (inability to reliably identify any abnormality in patients who have only a partial loss of vestibular function). A recent study demonstrated that VOR gain measures from rotation tests using both velocity step and sum-of-sines stimuli were uncorrelated with the severity of unilateral vestibular dysfunction as characterized by the caloric RVR measure (See reference 57 listed below). The mean VOR time constant, determined from velocity step responses and indirectly from responses to sum-of-sines stimuli, did show a consistent decline with increasing caloric RVR. However, the wide variability of results indicate that many patients with a 40-60% caloric RVR, and some with a 60-80% RVR, would not be distinguished from a normal population using conventional rotation testing. In addition, neither of these rotation tests provided a reliable indication of the side of vestibular loss, except in the 80-100% RVR patient group where velocity step rotations showed a small asymmetry between VOR time constants determined during rotations toward and away from the absent side.
A third limitation of conventional rotation testing is the ambiguity between rotation test results in patients with a partial bilateral loss and a compensated unilateral loss (inability to distinguish between patients with a partial bilateral vestibular loss and a compensated unilateral vestibular loss of function). Both abnormalities produce a reduction in the VOR time constant and, equivalently, a low frequency phase advance. A partial bilateral vestibular loss may cause only a mild reduction in VOR gain such that the VOR gain may remain within the normal range while the VOR time constant is reduced. This pattern of normal gain and reduced time constant is indistinguishable from a compensated unilateral vestibular loss pattern.
Autorotation Test. In the autorotation test, the patient rotates the head side-to-side in synchrony with an audio tone cue while viewing a fixed visual target. The autorotation test evaluates the VOR at higher frequencies of head rotation (2-6 Hz) than those in conventional rotation tests. Testing has become standardized using commercially available systems. Tests are performed in the light with the subject instructed to gaze at a fixed visual target. An audio tone cues the test subject to oscillate his/her head in time with the tone. The tone cue begins at 0.5 Hz and continuously increases to 6 Hz in about 20 s. Head movements at lower frequencies are used to calibrate the eye movement recordings, and higher frequency VOR responses are quantified using spectral analysis techniques to calculate response gain and phase at frequencies of 2 to 6 Hz. Deviations of gain and phase responses from normal ranges are indicative of abnormal vestibular function.
Autorotation tests evaluate the VOR in a frequency range higher than either caloric or conventional rotation tests. Since VOR function in this higher frequency range is important for maintenance of clear vision during head movements, autorotation testing provides physiologically relevant information related to gaze stability. The equipment for this test is inexpensive and portable, particularly compared to conventional rotation testing. There have been claims that this test has high sensitivity, with some patients showing abnormalities on autorotation tests even though caloric results were normal.
Although this test has been in use for over 10 years, there is little consensus regarding its utility and reliability. A recent study (See reference 27 listed below) investigated autorotation test reliability in 12 normal subjects and concluded that “Unfortunately, the test-retest reliability of the VAT [vestibular autorotation test] is poor, and therefore it cannot be used routinely.” This result, however, was disputed by the originator of the VAT system (See reference 44 listed below). Potential factors contributing to poor reliability include: eye movement recording artifacts caused by rapid head movements (high head accelerations), imperfect measurements of head movements (imperfect monitoring of head motion) that produce inaccurate evaluations of vestibular function, inconsistent ability of subjects to achieve regular oscillations at higher frequencies, and analysis artifacts introduced by fast phase eye movements. Finally, the scientific literature on autorotation has focused on the detection of abnormal responses, but little information (little research) is available about the test's ability to localize vestibular dysfunction to one or both ears and to quantify the magnitude of the deficit.
Head impulse test. In the head impulse test, an examiner rotates a patient's head with a rapid, high acceleration rotation though an angle of about 20-30° while the patient attempts to maintain higher gaze on a fixed target. The examiner looks for corrective eye movements following the head rotation, indicating that vestibular function is deficient and unable to generate VOR eye movements that fully compensate for the head rotation. Typically, the rotation is about the head's vertical axis which stimulates primarily the horizontal canals. The patient attempts to maintain his/her gaze fixed on a target during this maneuver. In patients with severe canal paresis, the rotation towards the dysfunctional ear or ears produces an inadequate compensatory VOR. This inadequate VOR causes the eyes to move off target, with the result being that a visually guided corrective saccade is generated to reacquire the target at the conclusion of the head rotation. The presence of this corrective saccade is a convenient qualitative clinical sign indicating abnormal canal function. Alternatively, if eye movements are recorded during head rotations, the gain of the VOR can be calculated and used as an indicator of VOR function.
The main advantage of head impulse testing is that the qualitative version of the test (i.e. using the presence of a corrective saccade as a sign of abnormality) can be performed by a knowledgeable practitioner with no equipment. In cases where patients were known to have a complete unilateral loss of vestibular function, the test has been shown to have 100% sensitivity and specificity. In addition, recent research indicates that this technique can be extended to include head rotations about oblique axes that allow for evaluation of the vertical semicircular canals.
The chief disadvantage of head impulse testing is that it has recently been shown in a study to have poor sensitivity in cases of less severe canal paresis (See reference 7 listed below). This blinded study compared the results of conventional caloric testing with head impulse testing. In patients with severe canal paresis (75-100% RVR on caloric testing), head impulse testing showed abnormal results in 77% of these patients. However, head impulse testing revealed abnormalities in only 9.5% of patients with moderate paresis (50-75% RVR) and 0% of patients with mild paresis (25-50% RVR). Overall, it was concluded that head impulse testing was useful in detecting severe paresis, but could not serve as a replacement for the caloric test. Major limitations are that: (1) it doe not adequately identify mild-to-moderate vestibular dysfunction in a single ear, and (2) the test cannot be used in patients with any limitations in neck mobility (e.g. limitations due to whiplash, arthritis).
Perhaps the sensitivity of head impulse testing could be improved by the use of controlled rotations and accurate eye movement recordings that have been applied in research studies. However, clinical application of these improved techniques is problematic for two reasons. First, better control of rotations would probably require whole body rotations. A rotation device to accomplish this would need high torques to generate the high accelerations required for these tests. Rotation devices that are currently in most clinical vestibular laboratories do not have adequate torque. Second, the short duration of the head impulse requires an accurate method of recording eye movements at a high sampling rate. Currently, the search coil technique seems to be the only adequate technology available. However, search coils are inconvenient to apply in a clinical setting, have some risk associated with their use (i.e. corneal injury), and can only be used for short time periods.
Finally, patients with neck injury or other limitations in neck mobility cannot be tested using rapid head on body rotations. Patients in this category would include patients with balance complaints associated with accidents causing whiplash injuries, and elderly patients with limited mobility due to arthritic conditions.